Allele-specific knockdown of ALS-associated mutant TDP-43 in neural stem cells derived from induced pluripotent stem cells

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Nishimura, Agnes L ^a   Shum, Carole ^a   Scotter, Emma L ^a   Abdelgany, Amr ^a   Sardone, Valentina ^b   Wright, Jamie ^a   Lee, Youn Bok ^a   Chen, Han Jou ^a   Bilican, Bilada ^c   Carrasco, Monica ^d   Maniatis, Tom ^d   Chandran, Siddharthan ^c   Rogelj, Boris ^e   Gallo, Jean Marc ^a   Shaw, Christopher E ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF PAVIA   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Department of Biochemistry and Molecular Biophysics Columbia University ^*  (United States)

^e JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE; SMALL INTERFERING RNA; TAR DNA BINDING PROTEIN; VALINE; DNA BINDING PROTEIN; MESSENGER RNA; PROTEIN TDP-43;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CONTROLLED STUDY; CYTOSOL; DRUG EFFECT; DRUG SELECTIVITY; DRUG TARGETING; EMBRYO; GENE MUTATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MUTANT; NEURAL STEM CELL; PLURIPOTENT STEM CELL; RNA INTERFERENCE; ALLELE; AMINO ACID SUBSTITUTION; CELL INCLUSION; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY;

ALLELES; AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; INCLUSION BODIES; INDUCED PLURIPOTENT STEM CELLS; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL STEM CELLS; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84923333393     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091269     Document Type: Article

References (39)

1. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130-133. (Pubitemid 44547757)
2. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, et al. (2009) Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations. Acta Neuropathol 117: 15-18.
3. Lagier-Tourenne C, Cleveland DW (2009) Rethinking ALS: the FUS about TDP-43. Cell 136: 1001-1004.
4. Nishimura AL, Zupunski V, Troakes C, Kathe C, Fratta P, et al. (2010) Nuclear import impairment causes cytoplasmic trans-activation response DNA-binding protein accumulation and is associated with frontotemporal lobar degeneration. Brain 133: 1763-1771.
5. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14: 452-458.
6. Winton MJ, Igaz LM, Wong MM, Kwong LK, Trojanowski JQ, et al. (2008) Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. J Biol Chem 283: 13302-13309.
7. Zhang Y, Engelman J, Friedlander RM (2009) Allele-specific silencing of mutant Huntington's disease gene. J Neurochem 108: 82-90.
8. Nishimoto Y, Ito D, Yagi T, Nihei Y, Tsunoda Y, et al. (2010) Characterization of alternative isoforms and inclusion body of the TAR DNA-binding protein-43. J Biol Chem 285: 608-619.
9. Yang C, Tan W, Whittle C, Qiu L, Cao L, et al. (2010) The C-terminal TDP-43 fragments have a high aggregation propensity and harm neurons by a dominant-negative mechanism. PLoS One 5: e15878.
10. Che MX, Jiang YJ, Xie YY, Jiang LL, Hu HY (2011) Aggregation of the 35-kDa fragment of TDP-43 causes formation of cytoplasmic inclusions and alteration of RNA processing. FASEB J 25: 2344-2353.
11. Corrado L, Ratti A, Gellera C, Buratti E, Castellotti B, et al. (2009) High frequency of TARDBP gene mutations in Italian patients with amyotrophic lateral sclerosis. Hum Mutat 30: 688-694.
12. Mackenzie IR, Rademakers R, Neumann M (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9: 995-1007.
13. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319: 1668-1672. (Pubitemid 351432505)
14. Rutherford NJ, Zhang YJ, Baker M, Gass JM, Finch NA, et al. (2008) Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet 4: e1000193.
15. Tamaoka A, Arai M, Itokawa M, Arai T, Hasegawa M, et al. (2010) TDP-43 M337V mutation in familial amyotrophic lateral sclerosis in Japan. Intern Med 49: 331-334.
16. Tsai CP, Soong BW, Lin KP, Tu PH, Lin JL, et al. (2011) FUS, TARDBP, and SOD1 mutations in a Taiwanese cohort with familial ALS. Neurobiol Aging 32: 553 e513-521.
17. Ling SC, Albuquerque CP, Han JS, Lagier-Tourenne C, Tokunaga S, et al. (2010) ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc Natl Acad Sci U S A 107: 13318-13323.
18. Kabashi E, Lin L, Tradewell ML, Dion PA, Bercier V, et al. (2010) Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 19: 671-683.
19. Xu YF, Zhang YJ, Lin WL, Cao X, Stetler C, et al. (2011) Expression of mutant TDP-43 induces neuronal dysfunction in transgenic mice. Mol Neurodegener 6: 73.
20. de Ynigo-Mojado L, Martin-Ruiz I, Sutherland JD (2011) Efficient allele-specific targeting of LRRK2 R1441 mutations mediated by RNAi. PLoS One 6: e21352.
21. Rodriguez-Lebron E, Gouvion CM, Moore SA, Davidson BL, Paulson HL (2009) Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer's disease. Mol Ther 17: 1563-1573.
22. Miller VM, Gouvion CM, Davidson BL, Paulson HL (2004) Targeting Alzheimer's disease genes with RNA interference: an efficient strategy for silencing mutant alleles. Nucleic Acids Res 32: 661-668. (Pubitemid 38263057)
23. van Bilsen PH, Jaspers L, Lombardi MS, Odekerken JC, Burright EN, et al. (2008) Identification and allele-specific silencing of the mutant huntingtin allele in Huntington's disease patient-derived fibroblasts. Hum Gene Ther 19: 710-719.
24. Lombardi MS, Jaspers L, Spronkmans C, Gellera C, Taroni F, et al. (2009) A majority of Huntington's disease patients may be treatable by individualized allele-specific RNA interference. Exp Neurol 217: 312-319.
25. Fiszer A, Mykowska A, Krzyzosiak WJ (2011) Inhibition of mutant huntingtin expression by RNA duplex targeting expanded CAG repeats. Nucleic Acids Res 39: 5578-5585.
26. Ding H, Schwarz DS, Keene A, Affar el B, Fenton L, et al. (2003) Selective silencing by RNAi of a dominant allele that causes amyotrophic lateral sclerosis. Aging Cell 2: 209-217.
27. Maxwell MM, Pasinelli P, Kazantsev AG, Brown RH, Jr. (2004) RNA interference-mediated silencing of mutant superoxide dismutase rescues cyclosporin A-induced death in cultured neuroblastoma cells. Proc Natl Acad Sci U S A 101: 3178-3183. (Pubitemid 38327754)
28. Raoul C, Abbas-Terki T, Bensadoun JC, Guillot S, Haase G, et al. (2005) Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat Med 11: 423-428. (Pubitemid 40562333)
29. Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, et al. (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11: 429-433. (Pubitemid 40562334)
30. Towne C, Raoul C, Schneider BL, Aebischer P (2008) Systemic AAV6 delivery mediating RNA interference against SOD1: neuromuscular transduction does not alter disease progression in fALS mice. Mol Ther 16: 1018-1025. (Pubitemid 351737065)
31. Bilican B, Serio A, Barmada SJ, Nishimura AL, Sullivan GJ, et al. (2012) Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci U S A 109: 5803-5808.
32. Li W, Sun W, Zhang Y, Wei W, Ambasudhan R, et al. (2011) Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc Natl Acad Sci U S A 108: 8299-8304.
33. Scotter EL, Narayan P, Glass M, Dragunow M (2008) High throughput quantification of mutant huntingtin aggregates. J Neurosci Methods 171: 174-179.
34. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, et al. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498. (Pubitemid 32494397)
35. Abdelgany A, Wood M, Beeson D (2003) Allele-specific silencing of a pathogenic mutant acetylcholine receptor subunit by RNA interference. Hum Mol Genet 12: 2637-2644. (Pubitemid 37304686)
36. Ayala YM, De Conti L, Avendaño-Vázquez SE, Dhir A, Romano M, et al. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. The EMBO Journal 30: 277-288.
37. Kraemer B, Schuck T, Wheeler J, Robinson L, Trojanowski J, et al. (2010) Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathologica 119: 409-419.
38. Sephton CF, Good SK, Atkin S, Dewey CM, Mayer P, et al. (2009) TDP-43 Is a Developmentally Regulated Protein Essential for Early Embryonic Development. Journal of Biological Chemistry 285: 6826-6834.
39. Wu L-S, Cheng W-C, Hou S-C, Yan Y-T, Jiang S-T, et al. (2009) TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 48: 56-62.